Chromatin changes in SMARCAL1 deficiency: A hypothesis for the gene expression alterations of Schimke immuno-osseous dysplasia

References

• Boerkoel CF, Takashima H, John J, Yan J, Stankiewicz P, Rosenbarker L, Andre JL, Bogdanovic R, Burguet A, Cockfield S, et al. Mutant chromatin remodeling protein SMARCAL1 causes Schimke immuno-osseous dysplasia. Nat Genet 2002; 30:215-20; PMID:11799392; http://dx.doi.org/10.1038/ng821
   PubMed Web of Science ®Google Scholar
• Schimke RN, Horton WA, King CR. Chondroitin-6-sulphaturia, defective cellular immunity, and nephrotic syndrome. Lancet 1971; 2:1088-9; PMID:4106927; http://dx.doi.org/10.1016/S0140-6736(71)90400-4
   PubMed Web of Science ®Google Scholar
• Spranger J, Hinkel GK, Stoss H, Thoenes W, Wargowski D, Zepp F. Schimke immuno-osseous dysplasia: A newly recognized multisystem disease. J Pediatr 1991; 119:64-72; PMID:2066860; http://dx.doi.org/10.1016/S0022-3476(05)81040-6
   PubMed Web of Science ®Google Scholar
• Ehrich JH, Burchert W, Schirg E, Krull F, Offner G, Hoyer PF, Brodehl J. Steroid resistant nephrotic syndrome associated with spondyloepiphyseal dysplasia, transient ischemic attacks and lymphopenia. Clin Nephrol 1995; 43:89-95; PMID:7736684
   PubMed Web of Science ®Google Scholar
• Boerkoel CF, O'Neill S, Andre JL, Benke PJ, Bogdanovic R, Bulla M, Burguet A, Cockfield S, Cordeiro I, Ehrich JH, et al. Manifestations and treatment of Schimke immuno-osseous dysplasia: 14 new cases and a review of the literature. Eur J Pediatr 2000; 159:1-7; PMID:10653321; http://dx.doi.org/10.1007/s004310050001
   PubMed Web of Science ®Google Scholar
• Clewing JM, Antalfy BC, Lücke T, Najafian B, Marwedel KM, Hori A, Powel RM, Safo Do AF, Najera L, SantaCruz K, et al. Schimke immuno-osseous dysplasia: A clinicopathological correlation. J Med Genet 2007; 44:122-30; PMID:16840568; http://dx.doi.org/10.1136/jmg.2006.044313
   PubMed Web of Science ®Google Scholar
• Morimoto M, Yu Z, Stenzel P, Clewing JM, Najafian B, Mayfield C, Hendson G, Weinkauf JG, Gormley AK, Parham DM, et al. Reduced elastogenesis: A clue to the arteriosclerosis and emphysematous changes in Schimke immuno-osseous dysplasia? Orphanet J Rare Dis 2012; 7:70; PMID:22998683; http://dx.doi.org/10.1186/1750-1172-7-70
   PubMed Web of Science ®Google Scholar
• Morimoto M, Kerouredan O, Gendronneau M, Shuen C, Baradaran-Heravi A, Asakura Y, Basiratnia M, Bogdanovic R, Bonneau D, Buck A, et al. Dental abnormalities in Schimke immuno-osseous dysplasia. J Dent Res 2012; 91:29S-37S; PMID:22699664; http://dx.doi.org/10.1177/0022034512450299
   PubMedGoogle Scholar
• Lama G, Marrone N, Majorana M, Cirillo F, Salsano ME, Rinaldi MM. Spondyloepiphyseal dysplasia tarda and nephrotic syndrome in three siblings. Pediatr Nephrol 1995; 9:19-23; PMID:7742215; http://dx.doi.org/10.1007/BF00858959
   PubMed Web of Science ®Google Scholar
• Lou S, Lamfers P, McGuire N, Boerkoel CF. Longevity in Schimke immuno-osseous dysplasia. J Med Genet 2002; 39:922-5; PMID:12471207; http://dx.doi.org/10.1136/jmg.39.12.922
   PubMed Web of Science ®Google Scholar
• Lücke T, Billing H, Sloan EA, Boerkoel CF, Franke D, Zimmering M, Ehrich JH, Das AM. Schimke-immuno-osseous dysplasia: New mutation with weak genotype-phenotype correlation in siblings. Am J Med Genet A 2005; 135:202-5; PMID:15880370; http://dx.doi.org/10.1002/ajmg.a.30691
   PubMed Web of Science ®Google Scholar
• Clewing JM, Fryssira H, Goodman D, Smithson SF, Sloan EA, Lou S, Huang Y, Choi K, Lucke T, Alpay H, et al. Schimke immunoosseous dysplasia: Suggestions of genetic diversity. Hum Mutat 2007; 28:273-83; PMID:17089404; http://dx.doi.org/10.1002/humu.20432
   PubMed Web of Science ®Google Scholar
• Dekel B, Metsuyanim S, Goldstein N, Pode-Shakked N, Kovalski Y, Cohen Y, Davidovits M, Anikster Y. Schimke immuno-osseous dysplasia: Expression of SMARCAL1 in blood and kidney provides novel insight into disease phenotype. Pediatr Res 2008; 63:398-403; PMID:18356746; http://dx.doi.org/10.1203/PDR.0b013e31816721cc
   PubMed Web of Science ®Google Scholar
• Baradaran-Heravi A, Cho KS, Tolhuis B, Sanyal M, Morozova O, Morimoto M, Elizondo LI, Bridgewater D, Lubieniecka J, Beirnes K, et al. Penetrance of biallelic SMARCAL1 mutations is associated with environmental and genetic disturbances of gene expression. Hum Mol Genet 2012; 21:2572-87; PMID:22378147; http://dx.doi.org/10.1093/hmg/dds083
   PubMed Web of Science ®Google Scholar
• Postow L, Woo EM, Chait BT, Funabiki H. Identification of SMARCAL1 as a component of the DNA damage response. J Biol Chem 2009; 284:35951-61; PMID:19841479; http://dx.doi.org/10.1074/jbc.M109.048330
   PubMed Web of Science ®Google Scholar
• Yuan J, Ghosal G, Chen J. The annealing helicase HARP protects stalled replication forks. Genes Dev 2009; 23:2394-9; PMID:19793864; http://dx.doi.org/10.1101/gad.1836409
   PubMed Web of Science ®Google Scholar
• Yusufzai T, Kong X, Yokomori K, Kadonaga JT. The annealing helicase HARP is recruited to DNA repair sites via an interaction with RPA. Genes Dev 2009; 23:2400-4; PMID:19793863; http://dx.doi.org/10.1101/gad.1831509
   PubMed Web of Science ®Google Scholar
• Bansbach CE, Betous R, Lovejoy CA, Glick GG, Cortez D. The annealing helicase SMARCAL1 maintains genome integrity at stalled replication forks. Genes Dev 2009; 23:2405-14; PMID:19793861; http://dx.doi.org/10.1101/gad.1839909
   PubMed Web of Science ®Google Scholar
• Ciccia A, Bredemeyer AL, Sowa ME, Terret ME, Jallepalli PV, Harper JW, Elledge SJ. The SIOD disorder protein SMARCAL1 is an RPA-interacting protein involved in replication fork restart. Genes Dev 2009; 23:2415-25; PMID:19793862; http://dx.doi.org/10.1101/gad.1832309
   PubMed Web of Science ®Google Scholar
• Sanyal M, Morimoto M, Baradaran-Heravi A, Choi K, Kambham N, Jensen K, Dutt S, Dionis-Petersen KY, Liu LX, Felix K, et al. Lack of IL7Ralpha expression in T cells is a hallmark of T-cell immunodeficiency in Schimke immuno-osseous dysplasia (SIOD). Clin Immunol 2015; 161:355-65; PMID:26499378; http://dx.doi.org/10.1016/j.clim.2015.10.005
   PubMed Web of Science ®Google Scholar
• Morimoto M, Myung C, Beirnes K, Choi K, Asakura Y, Bokenkamp A, Bonneau D, Brugnara M, Charrow J, Colin E, et al. Increased Wnt and Notch signaling: A clue to the renal disease in Schimke immuno-osseous dysplasia? Orphanet J Rare Dis 2016; 11:149; PMID:27816064; http://dx.doi.org/10.1186/s13023-016-0519-7
   Web of Science ®Google Scholar
• Bell O, Tiwari VK, Thoma NH, Schubeler D. Determinants and dynamics of genome accessibility. Nat Rev Genet 2011; 12:554-64; PMID:21747402; http://dx.doi.org/10.1038/nrg3017
   PubMed Web of Science ®Google Scholar
• Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 2007; 128:735-45; PMID:17320510; http://dx.doi.org/10.1016/j.cell.2007.02.009
   PubMed Web of Science ®Google Scholar
• Steffen PA, Ringrose L. What are memories made of? How Polycomb and Trithorax proteins mediate epigenetic memory. Nat Rev Mol Cell Biol 2014; 15:340-56; PMID:24755934; http://dx.doi.org/10.1038/nrm3789
   PubMed Web of Science ®Google Scholar
• Pearson JC, Lemons D, McGinnis W. Modulating Hox gene functions during animal body patterning. Nat Rev Genet 2005; 6:893-904; PMID:16341070; http://dx.doi.org/10.1038/nrg1726
   PubMed Web of Science ®Google Scholar
• Saget O, Randsholt NB. Transposon-induced rearrangements in the duplicated locus ph of Drosophila melanogaster can create new chimeric genes functionally identical to the wild type. Gene 1994; 149:227-35; PMID:7958995; http://dx.doi.org/10.1016/0378-1119(94)90154-6
   PubMed Web of Science ®Google Scholar
• Tiong SY, Russell MA. Clonal analysis of segmental and compartmental homoeotic transformations in polycomb mutants of Drosophila melanogaster. Dev Biol 1990; 141:306-18; PMID:1976555; http://dx.doi.org/10.1016/0012-1606(90)90387-X
   PubMed Web of Science ®Google Scholar
• Tearle RG, Nusslein-Volhard C. Tubingen mutants and stock list. Drosoph Inf Serv 1987; 66:209-69
   Google Scholar
• Ruhf ML, Braun A, Papoulas O, Tamkun JW, Randsholt N, Meister M. The domino gene of Drosophila encodes novel members of the SWI2/SNF2 family of DNA-dependent ATPases, which contribute to the silencing of homeotic genes. Development 2001; 128:1429-41; PMID:11262242
   PubMed Web of Science ®Google Scholar
• Ingham PW, Whittle R. Trithorax: A new homeotic mutation of Drosophila melanogaster causing transformations of abdominal and thoracic imaginal segments. Mol Gen Genet 1980; 179:607-14; http://dx.doi.org/10.1007/BF00271751
   Google Scholar
• Kennison JA, Tamkun JW. Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc Natl Acad Sci U S A 1988; 85:8136-40; PMID:3141923; http://dx.doi.org/10.1073/pnas.85.21.8136
   PubMed Web of Science ®Google Scholar
• Chan CS, Rastelli L, Pirrotta V. A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J 1994; 13:2553-64; PMID:7912192
   PubMed Web of Science ®Google Scholar
• Tillib S, Petruk S, Sedkov Y, Kuzin A, Fujioka M, Goto T, Mazo A. Trithorax- and Polycomb-group response elements within an Ultrabithorax transcription maintenance unit consist of closely situated but separable sequences. Mol Cell Biol 1999; 19:5189-202; PMID:10373568; http://dx.doi.org/10.1128/MCB.19.7.5189
   PubMed Web of Science ®Google Scholar
• Lewis EB. A gene complex controlling segmentation in Drosophila. Nature 1978; 276:565-70; PMID:103000; http://dx.doi.org/10.1038/276565a0
   PubMed Web of Science ®Google Scholar
• Lewis EB. Genes and developmental pathways. Am Zool 1963; 3:33-56; http://dx.doi.org/10.1093/icb/3.1.33
   Google Scholar
• van der Knaap JA, Kumar BR, Moshkin YM, Langenberg K, Krijgsveld J, Heck AJ, Karch F, Verrijzer CP. GMP synthetase stimulates histone H2B deubiquitylation by the epigenetic silencer USP7. Mol Cell 2005; 17:695-707; PMID:15749019; http://dx.doi.org/10.1016/j.molcel.2005.02.013
   PubMed Web of Science ®Google Scholar
• White RAH, Akam ME. Contrabithorax mutations cause inappropriate expression of Ultrabithorax products in Drosophila. Nature 1985; 318:567-70; http://dx.doi.org/10.1038/318567a0
   Web of Science ®Google Scholar
• Fritsch C, Brown JL, Kassis JA, Muller J. The DNA-binding polycomb group protein pleiohomeotic mediates silencing of a Drosophila homeotic gene. Development 1999; 126:3905-13; PMID:10433918
   PubMed Web of Science ®Google Scholar
• Papp B, Muller J. Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev 2006; 20:2041-54; PMID:16882982; http://dx.doi.org/10.1101/gad.388706
   PubMed Web of Science ®Google Scholar
• Schiavone D, Guilbaud G, Murat P, Papadopoulou C, Sarkies P, Prioleau MN, Balasubramanian S, Sale JE. Determinants of G quadruplex-induced epigenetic instability in REV1-deficient cells. EMBO J 2014; 33:2507-20; PMID:25190518; http://dx.doi.org/10.15252/embj.201488398
   PubMed Web of Science ®Google Scholar
• Papadopoulou C, Guilbaud G, Schiavone D, Sale JE. Nucleotide pool depletion induces G-quadruplex-dependent perturbation of gene expression. Cell Rep 2015; 13:2491-503; PMID:26686635; http://dx.doi.org/10.1016/j.celrep.2015.11.039
   PubMed Web of Science ®Google Scholar
• Khurana S, Oberdoerffer P. Replication stress: A lifetime of epigenetic change. Genes (Basel) 2015; 6:858-77; PMID:26378584
   PubMed Web of Science ®Google Scholar
• Kim HR, Hwang KA, Kim KC, Kang I. Down-regulation of IL-7Ralpha expression in human T cells via DNA methylation. J Immunol 2007; 178:5473-9; PMID:17442928; http://dx.doi.org/10.4049/jimmunol.178.9.5473
   PubMed Web of Science ®Google Scholar
• Tamkun JW, Deuring R, Scott MP, Kissinger M, Pattatucci AM, Kaufman TC, Kennison JA. brahma: A regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 1992; 68:561-72; PMID:1346755; http://dx.doi.org/10.1016/0092-8674(92)90191-E
   PubMed Web of Science ®Google Scholar
• Elfring LK, Daniel C, Papoulas O, Deuring R, Sarte M, Moseley S, Beek SJ, Waldrip WR, Daubresse G, DePace A, et al. Genetic analysis of brahma: The Drosophila homolog of the yeast chromatin remodeling factor SWI2/SNF2. Genetics 1998; 148:251-65; PMID:9475737
   PubMed Web of Science ®Google Scholar
• Papoulas O, Daubresse G, Armstrong JA, Jin J, Scott MP, Tamkun JW. The HMG-domain protein BAP111 is important for the function of the BRM chromatin-remodeling complex in vivo. Proc Natl Acad Sci U S A 2001; 98:5728-33; PMID:11331758; http://dx.doi.org/10.1073/pnas.091533398
   PubMed Web of Science ®Google Scholar
• Di Croce L, Helin K. Transcriptional regulation by Polycomb group proteins. Nat Struct Mol Biol 2013; 20:1147-55; PMID:24096405; http://dx.doi.org/10.1038/nsmb.2669
   PubMed Web of Science ®Google Scholar
• Keene MA, Elgin SC. Micrococcal nuclease as a probe of DNA sequence organization and chromatin structure. Cell 1981; 27:57-64; PMID:6799212; http://dx.doi.org/10.1016/0092-8674(81)90360-3
   PubMed Web of Science ®Google Scholar
• Levy A, Noll M. Chromatin fine structure of active and repressed genes. Nature 1981; 289:198-203; PMID:6779207; http://dx.doi.org/10.1038/289198a0
   PubMed Web of Science ®Google Scholar
• Aygun O, Svejstrup J, Liu Y. A RECQ5-RNA polymerase II association identified by targeted proteomic analysis of human chromatin. Proc Natl Acad Sci U S A 2008; 105:8580-4; PMID:18562274; http://dx.doi.org/10.1073/pnas.0804424105
   PubMed Web of Science ®Google Scholar
• Jeronimo C, Langelier MF, Zeghouf M, Cojocaru M, Bergeron D, Baali D, Forget D, Mnaimneh S, Davierwala AP, Pootoolal J, et al. RPAP1, a novel human RNA polymerase II-associated protein affinity purified with recombinant wild-type and mutated polymerase subunits. Mol Cell Biol 2004; 24:7043-58; PMID:15282305; http://dx.doi.org/10.1128/MCB.24.16.7043-7058.2004
   PubMed Web of Science ®Google Scholar
• Robert F, Blanchette M, Maes O, Chabot B, Coulombe B. A human RNA polymerase II-containing complex associated with factors necessary for spliceosome assembly. J Biol Chem 2002; 277:9302-6; PMID:11773074; http://dx.doi.org/10.1074/jbc.M110516200
   PubMed Web of Science ®Google Scholar
• Sharma T, Bansal R, Haokip DT, Goel I, Muthuswami R. SMARCAL1 negatively regulates c-Myc transcription by altering the conformation of the promoter region. Sci Rep 2015; 5:17910; PMID:26648259; http://dx.doi.org/10.1038/srep17910
   PubMed Web of Science ®Google Scholar
• Morimoto M, Wang KJ, Yu Z, Gormley AK, Parham D, Bogdanovic R, Lucke T, Mayfield C, Weksberg R, Hendson G, et al. Transcriptional and posttranscriptional mechanisms contribute to the dysregulation of elastogenesis in Schimke immuno-osseous dysplasia. Pediatr Res 2015; 78:609-17; PMID:26309238; http://dx.doi.org/10.1038/pr.2015.156
   PubMed Web of Science ®Google Scholar
• Fousteri M, Mullenders LH. Transcription-coupled nucleotide excision repair in mammalian cells: Molecular mechanisms and biological effects. Cell Res 2008; 18:73-84; PMID:18166977; http://dx.doi.org/10.1038/cr.2008.6
   PubMed Web of Science ®Google Scholar
• Keka IS, Mohiuddin  , Maede Y, Rahman MM, Sakuma T, Honma M, Yamamoto T, Takeda S, Sasanuma H. Smarcal1 promotes double-strand-break repair by nonhomologous end-joining. Nucleic Acids Res 2015; 43:6359-72; PMID:26089390; http://dx.doi.org/10.1093/nar/gkv621
   PubMed Web of Science ®Google Scholar
• Baradaran-Heravi A, Raams A, Lubieniecka J, Cho KS, DeHaai KA, Basiratnia M, Mari PO, Xue Y, Rauth M, Olney AH, et al. SMARCAL1 deficiency predisposes to non-Hodgkin lymphoma and hypersensitivity to genotoxic agents in vivo. Am J Med Genet A 2012; 158A:2204-13; PMID:22888040; http://dx.doi.org/10.1002/ajmg.a.35532
   PubMed Web of Science ®Google Scholar
• Zeman MK, Cimprich KA. Causes and consequences of replication stress. Nat Cell Biol 2014; 16:2-9; PMID:24366029; http://dx.doi.org/10.1038/ncb2897
   PubMed Web of Science ®Google Scholar
• Baradaran-Heravi A, Morimoto M, Tolhuis B, Shaw C, Sanyal M, Raams A, Bokenkamp A, Cho KS, Myung C, Leung D, et al. Schimke immuno-osseous dysplasia: A Mendelian complex trait arising from impaired DNA maintenance and global alterations in gene expression. 60th Annual American Society of Human Genetics Meeting, November 2–6, 2010, Washington, DC, United States.
   Google Scholar
• Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993; 118:401-15; PMID:8223268
   PubMed Web of Science ®Google Scholar
• Cavalli G, Orlando V, Paro R. Mapping DNA target sites of chromatin-associated proteins by formaldehyde cross-linking in Drosophila embryos. In: Bickmore WA, ed. Chromosome Structural Analysis: A Practical Approach. Oxford: Oxford University Press, 1999:20-37
   Google Scholar
• Wang L, Brown JL, Cao R, Zhang Y, Kassis JA, Jones RS. Hierarchical recruitment of polycomb group silencing complexes. Mol Cell 2004; 14:637-46; PMID:15175158; http://dx.doi.org/10.1016/j.molcel.2004.05.009
   PubMed Web of Science ®Google Scholar
• Tolhuis B, de Wit E, Muijrers I, Teunissen H, Talhout W, van Steensel B, van Lohuizen M. Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat Genet 2006; 38:694-9; PMID:16628213; http://dx.doi.org/10.1038/ng1792
   PubMed Web of Science ®Google Scholar
• Ner SS, Harrington MJ, Grigliatti TA. A role for the Drosophila SU(VAR)3-9 protein in chromatin organization at the histone gene cluster and in suppression of position-effect variegation. Genetics 2002; 162:1763-74; PMID:12524347
   PubMed Web of Science ®Google Scholar